Are We Smart Enough to Know How Smart Animals Are

by Frans de Waal

  The lesson is that before scientists test any animal, they need to know its typical behavior. The power of conditioning is not in doubt, but the early investigators had totally overlooked a crucial piece of information. They had not, as recommended by Lorenz, considered the whole organism. Animals show many unconditioned responses, or behavior that develops naturally in all members of their species. Reward and punishment may affect such behavior but cannot take credit creating it. The reason all cats responded in the same way derived from natural feline communication rather than operant conditioning.

  The field of evolutionary cognition requires us to consider every species in full. Whether we are studying hand anatomy, trunk multifunctionality, face perception, or greeting rituals, we need to familiarize ourselves with all facets of the animal and its natural history before trying to figure out its mental level. And instead of testing animals on abilities that we are particularly good at—our own species’ magic wells, such as language—why not test them on their specialized skills? In doing so, we will not just flatten Aristotle’s scale of nature: we will transform it into a bush with many branches. This change in perspective is now feeding the long-overdue recognition that intelligent life is not something we must seek at great expense only in the outer reaches of space. It is abundant here on earth, right underneath our nonprehensile noses.18

  Anthropodenial

  The ancient Greeks believed that the center of the universe was right where they lived. What better place, therefore, than Greece for modern scholars to ponder humanity’s place in the cosmos? On a sunny day in 1996, an international group of academics visited the omphalos (navel) of the world—a large stone shaped like a beehive—amid the temple ruins on Mount Parnassus. I couldn’t resist patting it like a long-lost friend. Right next to me stood “batman” Don Griffin, the discoverer of echolocation and author of The Question of Animal Awareness, in which he lamented the misperception that everything in the world turns around us and that we are the only conscious beings.19

  Ironically, a major theme of our workshop was the anthropic principle, according to which the universe is a purposeful creation uniquely suited for intelligent life, meaning us.20 At times the discourse of the anthropic philosophers sounded as if they thought the world was made for us rather than the other way around. Planet Earth is at exactly the right distance from the sun to create the right temperature for human life, and its atmosphere has the ideal oxygen level. How convenient! Instead of seeing purpose in this situation, however, any biologist will turn the causal connection around and note that our species is finely adapted to the planet’s circumstances, which explains why they are perfect for us. Deep ocean vents are an optimal environment for bacteria thriving on their superhot sulfuric output, but no one assumes that these vents were created to serve thermophile bacteria; rather, we understand that natural selection has shaped bacteria able to live near them.

  The backward logic of these philosophers reminded me of a creationist I once saw peel a banana on television while explaining that this fruit is curved in such a way that it conveniently angles toward the human mouth when we hold it in our hand. It also fits perfectly in our mouth. Obviously, he felt that God had given the banana its human-friendly shape, while forgetting that he was holding a domesticated fruit, cultivated for human consumption.

  During some of these discussions, Don Griffin and I watched barn swallows flying back and forth outside the conference room window carrying mouthfuls of mud for their nests. Griffin was at least three decades my senior and had impressive knowledge, offering the Latin name of the birds and describing details of their incubation period. At the workshop, he presented his view on consciousness: that it has to be part and parcel of all cognitive processes, including those of animals. My own position is slightly different in that I prefer not to make any firm statements about something as poorly defined as consciousness. No one seems to know what it is. But for the same reason, I hasten to add, I’d never deny it to any species. For all I know, a frog may be conscious. Griffin took a more positive stance, saying that since intentional, intelligent actions are observable in many animals, and since in our own species they go together with awareness, it is reasonable to assume similar mental states in other species.

  That such a highly respected and accomplished scientist made this claim had a hugely liberating effect. Even though Griffin was slammed for making statements that he could not back up with data, many critics missed the point, which was that the assumption that animals are “dumb,” in the sense that they lack conscious minds, is only that: an assumption. It is far more logical to assume continuity in every domain, Griffin said, echoing Charles Darwin’s well-known observation that the mental difference between humans and other animals is one of degree rather than kind.

  Ape gestures are homologous with those of humans. Not only do they look strikingly human, they occur in roughly similar contexts. Here a female chimpanzee (right) kisses a grizzled alpha male on the mouth during a reconciliation after a fight between them.

  It was an honor to get to know this kindred spirit and to make my own case regarding anthropomorphism, another theme at the conference. Greek for “human form,” the word anthropomorphism came about when Xenophanes, in 570 B.C., objected to Homer’s poetry because it described the gods as if they looked like people. Xenophanes ridiculed the arrogance behind this assumption—why couldn’t they look like horses? But gods are gods, far removed from the present-day liberal use of the word anthropomorphism as an epithet to vilify any and all human-animal comparisons, even the most cautious ones.

  In my opinion, anthropomorphism is problematic only when the human-animal comparison is a stretch, such as with regards to species distant from us. The fish known as kissing gouramis, for example, don’t really kiss in the same way and for the same reasons that humans do. Adult fish sometimes lock their protruding mouths together to settle disputes. Clearly, to label this habit “kissing” is misleading. Apes, on the other hand, do greet each other after a separation by placing their lips gently on each other’s mouth or shoulder and hence kiss in a way and under circumstances that greatly resemble human kissing. Bonobos go even further: when a zookeeper familiar with chimpanzees once naïvely accepted a bonobo kiss, not knowing this species, he was taken aback by the amount of tongue that went into it!

  Another example: when young apes are being tickled, they make breathy sounds with a rhythm of inhalation and exhalation that resembles human laughter. One cannot simply dismiss the term laughter for this behavior as too anthropomorphic (as some have done), because not only do the apes sound like human children being tickled, they show the same ambivalence about it as children do. I have often noticed it myself. They try to push my tickling fingers away, but then come back begging for more, holding their breath while awaiting the next poke in their belly. In this case, I am all for shifting the burden of proof and ask those who wish to avoid humanlike terminology to first prove that a tickled ape, who almost chokes on its hoarse giggles, is in fact in a different state of mind from a tickled human child. Absent such evidence, laughter strikes me as the best label for both.21

  Needing a new term to make my point, I invented anthropodenial, which is the a priori rejection of humanlike traits in other animals or animallike traits in us. Anthropomorphism and anthropodenial have an inverse relationship: the closer another species is to us, the more anthropomorphism will assist our understanding of this species and the greater will be the danger of anthropodenial.22 Conversely, the more distant a species is from us, the greater the risk that anthropomorphism will propose questionable similarities that have come about independently. Saying that ants have “queens,” “soldiers,” and “slaves” is mere anthropomorphic shorthand. We should attach no more significance to it than we do when we name a hurricane after a person or curse our computer as if it had free will.

  The key point is that anthropomorphism is not always as problematic as people think. To rail against it for the sake of scientific objecti
vity often hides a pre-Darwinian mindset, one uncomfortable with the notion of humans as animals. When we are considering species like the apes, which are aptly known as “anthropoids” (humanlike), however, anthropomorphism is in fact a logical choice. Dubbing an ape’s kiss “mouth-to-mouth contact” so as to avoid anthropomorphism deliberately obfuscates the meaning of the behavior. It would be like assigning Earth’s gravity a different name than the moon’s, just because we think Earth is special. Unjustified linguistic barriers fragment the unity with which nature presents us. Apes and humans did not have enough time to independently evolve strikingly similar behavior, such as lip contact in greeting or noisy breathing in response to tickling. Our terminology should honor the obvious evolutionary connections.

  On the other hand, anthropomorphism would be a rather empty exercise if all it did was paste human labels onto animal behavior. The American biologist and herpetologist Gordon Burghardt has called for a critical anthropomorphism, in which we use human intuition and knowledge of an animal’s natural history to formulate research questions.23 Thus, saying that animals “plan” for the future or “reconcile” after fights is more than anthropomorphic language: these terms propose testable ideas. If primates are capable of planning, for example, they should hold on to a tool that they can use only in the future. And if primates reconcile after fights, we should see a reduction of tensions as well as improved social relationships after opponents have made up by means of friendly contact. These obvious predictions have by been borne out by actual experiments and observations.24 Serving as a means rather than an end, critical anthropomorphism is a valuable source of hypotheses.

  Griffin’s proposal to take animal cognition seriously led to a new label for this field: cognitive ethology. It is a great label, but then I am an ethologist and know exactly what he meant. Unfortunately, the term ethology has not universally caught on, and spell-checkers still regularly change it to ethnology, etiology, or even theology. No wonder many ethologists nowadays call themselves behavioral biologists. Other existing labels for cognitive ethology are animal cognition and comparative cognition. But those two terms have drawbacks, too. Animal cognition fails to include humans, so it unintentionally perpetuates the idea of a gap between humans and other animals. The comparative label, on the other hand, remains agnostic about how and why we make comparisons. It hints at no framework whatsoever to interpret similarities and differences, least of all an evolutionary one. Even within this discipline, there have been complaints about its lack of theory as well as its habit of dividing animals into “higher” and “lower” forms.25 The label derives from comparative psychology, the name of a field that traditionally has viewed animals as mere stand-ins for humans: a monkey is a simplified human, a rat a simplified monkey, and so on. Since associative learning was thought to explain behavior across all species, one of the field’s founders, B. F. Skinner, felt that it hardly mattered what kind of animal one worked on.26 To prove his point, he entitled a book entirely devoted to albino rats and pigeons The Behavior of Organisms.

  For these reasons, Lorenz once joked that there was nothing comparative about comparative psychology. He knew what he was talking about, having just published a seminal study on the courtship patterns of twenty different duck species.27 His sensitivity to the minutest differences between species was quite the opposite of the way comparative psychologists lump animals together as “nonhuman models of human behavior.” Think for a second about this terminology, which remains so entrenched in psychology that no one takes notice anymore. Its first implication, of course, is that the only reason to study animals is to learn about ourselves. Second, it ignores that every species is uniquely adapted to its own ecology, because otherwise how could one serve as a model for another? Even the term nonhuman grates on me, since it lumps millions of species together by an absence, as if they were missing something. Poor things, they are nonhuman! When students embrace this jargon in their writing, I cannot resist sarcastic corrections in the margin saying that for completeness’s sake, they should add that the animals they are talking about are also nonpenguin, nonhyena, and a whole lot more.

  Even though comparative psychology is changing for the better, I’d rather avoid its leaden baggage and propose to call the new field evolutionary cognition, which is the study of all cognition (human and animal) from an evolutionary standpoint. Which species we study obviously matters a great deal, and humans are not necessarily central to every comparison. The field includes phylogeny, when we trace traits across the evolutionary tree to determine whether similarities are due to common descent, the way Lorenz had done so beautifully for waterfowl. We also ask how cognition has been shaped to serve survival. The agenda of this field is precisely what Griffin and Uexküll had in mind, in that it seeks to place the study of cognition on a less anthropocentric footing. Uexküll urged us to look at the world from the animal’s standpoint, saying that this is the only way to fully appreciate animal intelligence.

  A century later we are ready to listen.

  2 A TALE OF TWO SCHOOLS

  Do Dogs Desire?

  Given the prominent role that jackdaws and little silvery fish known as three-spined sticklebacks—my favorite childhood animals—played in the early years of ethology, the discipline was an easy sell to me. I learned about it when, as a biology student, I heard a professor explain the zigzag dance of the stickleback. I was floored: not by what these little fish did but by how seriously science took what they did. It was the first time I realized that what I liked doing best—watching animals behave—could be a profession. As a boy, I had spent hours observing self-caught aquatic life that I kept in buckets and tanks in our backyard. The high point had been breeding sticklebacks and releasing the young back into the ditch from which their parents had come.

  Ethology is the biological study of animal behavior that arose in continental Europe right before and after World War II. It reached the English-speaking world when one of its founders, Niko Tinbergen, moved across the Channel. A Dutch zoologist, Tinbergen started out in Leiden and accepted a position in Oxford in 1949. He described the male stickleback’s zigzag dance in great detail, explaining how it draws the female to the nest where the male fertilizes her eggs. The male then chases her off and protects the eggs, fanning and aerating them, until they hatch. I had seen it all with my own eyes in an abandoned aquarium—its luxurious algae growth was exactly what the fish needed—including the stunning transformation of silvery males into brightly red and blue show-offs. Tinbergen had noticed that males in tanks in the windowsill of his lab in Leiden would get agitated every time a red mail truck drove by in the street below. Using fish models to trigger courtship and aggression, he confirmed the critical role of a red signal.

  Clearly, ethology was the direction I wanted to go in, but before pursuing this goal, I was briefly diverted by its rival discipline. I worked in the lab of a psychology professor trained in the behaviorist tradition that dominated comparative psychology for most of the last century. This school was chiefly American but evidently had reached my university in the Netherlands. I still remember this professor’s classes, in which he made fun of anyone who believed to know what animals “want,” “like,” or “feel,” carefully neutralizing such terminology with quotation marks. If your dog drops a tennis ball in front of you and looks up at you with wagging tail, do you think she wants to play? How naïve! Who says dogs have desires and intentions? Her behavior is the product of the law of effect: she must have been rewarded for it in the past. The dog’s mind, if such a thing even exists, remains a black box.

  Its focus on nothing but behavior is what gave behaviorism its name, but I had trouble with the idea that animal behavior could be reduced to a history of incentives. It presented animals as passive, whereas I view them as seeking, wanting, and striving. True, their behavior changes based on its consequences, but they never act randomly or accidentally to begin with. Let’s take the dog and her ball. Throw a ball at a puppy, and she will go after
it like an eager predator. The more she learns about prey and their escape tactics—or about you and your fake throws—the better a hunter or fetcher she will become. But still, at the root of everything is her immense enthusiasm for the pursuit, which takes her through shrubs, into water, and sometimes through glass doors. This enthusiasm manifests itself before any skill development.

  Now, compare this behavior with that of your pet rabbit. It doesn’t matter how many balls your throw at him, none of the same learning will take place. Absent a hunting instinct, what is there to acquire? Even if you were to offer your rabbit a juicy carrot for every retrieved ball, you’d be in for a long, tedious training program that would never generate the excitement for small moving objects known of cats and dogs. Behaviorists totally overlooked these natural proclivities, forgetting that by flapping their wings, digging holes, manipulating sticks, gnawing wood, climbing trees, and so on, every species sets up its own learning opportunities. Many animals are driven to learn the things they need to know or do, the way kid goats practice head buts or human toddlers have an insuppressible urge to stand up and walk. This holds even for animals in a sterile box. It is no accident that rats are trained to press bars with their paws, pigeons to peck keys with their beaks, and cats to rub their flanks against a latch. Operant conditioning tends to reinforce what is already there. Instead of being the omnipotent creator of behavior, it is its humble servant.

  One of the first illustrations came from the work on kittiwakes by Esther Cullen, a postdoctoral student of Tinbergen. Kittiwakes are seabirds of the gull family; they differ from other gulls in that to deter predators, they nest on narrow cliffs. These birds rarely give alarm calls and do not vigorously defend their nests—they don’t need to. But what is most intriguing is that kittiwakes fail to recognize their young. Ground-nesting gulls, in which the young move around after hatching, recognize their offspring within days and do not hesitate to kick out strange ones that scientists place in their nests. Kittiwakes, on the other hand, can’t tell the difference between their own and strange young, treating the latter like their own. Not that they need to worry about this situation: fledglings normally stay put at the parental nest. This is, of course, precisely why biologists think kittiwakes lack individual recognition.1